Target organ damage and incident type 2 diabetes mellitus: the Strong Heart Study

Giovanni de Simone, Wenyu Wang, Lyle G Best, Fawn Yeh, Raffaele Izzo, Costantino Mancusi, Mary J Roman, Elisa T Lee, Barbara V Howard, Richard B Devereux, Giovanni de Simone, Wenyu Wang, Lyle G Best, Fawn Yeh, Raffaele Izzo, Costantino Mancusi, Mary J Roman, Elisa T Lee, Barbara V Howard, Richard B Devereux

Abstract

Background: Recent analyses in a registry of hypertensive patients suggested that preceding left ventricular (LV) hypertrophy (LVH) and/or carotid atherosclerosis are associated with incident type 2 diabetes, independent of confounders. We assess the relation between prevalent cardio-renal target organ damage (TOD) and subsequent incident type 2 diabetes in a population-based study with high prevalence of obesity.

Methods: We selected 2887 non-diabetic participants from two cohorts of the Strong Heart Study (SHS). Clinical exam, laboratory tests and echocardiograms were performed. Adjudicated TODs were LVH, left atrium (LA) dilatation, and high urine albumin/creatinine ratio (UACR). Multivariable logistic regression models were used to identify variables responsible for the association between initial TODs and incident diabetes at 4-year follow-up (FU).

Results: After 4 years, 297 new cases of diabetes (10%) were identified, 216 of whom exhibited baseline impaired fasting glucose (IFG, 73%, p < 0.0001). Participants developing type 2 diabetes exhibited higher inflammatory markers, fat-free mass and adipose mass and higher prevalence of initial LVH and LA dilatation than those without (both p < 0.04). In multivariable logistic regression, controlling for age, sex, family relatedness, presence of arterial hypertension and IFG, all three indicators of TOD predicted incident diabetes (all p < 0.01). However, the effects of TOD was offset when body fat and inflammatory markers were introduced into the model.

Conclusions: In this population-based study with high prevalence of obesity, TOD precedes clinical appearance of type 2 diabetes and is related to the preceding metabolic status, body composition and inflammatory status. Trial registration Trial registration number: NCT00005134, Name of registry: Strong Heart Study, URL of registry: https://ichgcp.net/clinical-trials-registry/NCT00005134, Date of registration: May 25, 2000, Date of enrolment of the first participant to the trial: September 1988.

Keywords: Arterial hypertension; Body composition; Inflammation; Left atrial dilatation; Left ventricular hypertrophy; Target organ damage.

Figures

Fig. 1
Fig. 1
Selection of the study population from the original cohort of non-diabetic participants to the Strong Heart Study and the Strong Heart Family Study
Fig. 2
Fig. 2
Risk of development of diabetes (expressed as OR and 95% of confidence interval) based on three indicator of target organ damage: LV hypertrophy (white circles), LA dilatation (grey circles) and high urinary albumin/creatinine excretion (black circle). All p value <0.05 except in Model 4

References

    1. de Simone G, Devereux RB, Roman MJ, Chinali M, Barac A, Panza JA, Lee ET, Galloway JM, Howard BV. Does cardiovascular phenotype explain the association between diabetes and incident heart failure? The Strong Heart Study. Nutr Metab Cardiovasc Dis. 2013;23(4):285–291. doi: 10.1016/j.numecd.2011.06.007.
    1. Devereux RB, Roman MJ, Paranicas M, O’Grady MJ, Lee ET, Welty TK, Fabsitz RR, Robbins D, Rhoades ER, Howard BV. Impact of diabetes on cardiac structure and function: the strong heart study. Circulation. 2000;101(19):2271–2276. doi: 10.1161/01.CIR.101.19.2271.
    1. Cioffi G, Faggiano P, Lucci D, Di LA, Mureddu GF, Tarantini L, Verdecchia P, Comaschi M, Giorda CB, Velussi M, et al. Inappropriately high left ventricular mass in patients with type 2 diabetes mellitus and no overt cardiac disease. The DYDA Study. J Hypertens. 2011;29(10):1994–2003. doi: 10.1097/HJH.0b013e32834acc6d.
    1. de Simone G, Devereux RB, Roman MJ, Schlussel Y, Alderman MH, Laragh JH. Echocardiographic left ventricular mass and electrolyte intake predict arterial hypertension. Ann Intern Med. 1991;114(3):202–209. doi: 10.7326/0003-4819-114-3-202.
    1. Izzo R, de Simone G, Devereux RB, Giudice R, De MM, Cimmino CS, Vasta A, De Luca N, Trimarco B. Initial left-ventricular mass predicts probability of uncontrolled blood pressure in arterial hypertension. J Hypertens. 2011;29(4):803–808. doi: 10.1097/HJH.0b013e328343ce32.
    1. Izzo R, de Simone G, Trimarco V, Gerdts E, Giudice R, Vaccaro O, De Luca N, Trimarco B. Hypertensive target organ damage predicts incident diabetes mellitus. Eur Heart J. 2013;34(44):3419–3426. doi: 10.1093/eurheartj/eht281.
    1. Howard BV, Lee ET, Cowan LD, Devereux RB, Galloway JM, Go OT, Howard WJ, Rhoades ER, Robbins DC, Sievers ML, et al. Rising tide of cardiovascular disease in American Indians. The Strong Heart Study. Circulation. 1999;99(18):2389–2395. doi: 10.1161/01.CIR.99.18.2389.
    1. Lee ET, Fabsitz R, Cowan LD, Le NA, Oopik AJ, Cucchiara AJ, Savage PJ, Howard BV, The Strong Heart Study A study of cardiovascular disease in American Indians: design and methods. Am J Epidemiol. 1990;136:1141–1155. doi: 10.1093/oxfordjournals.aje.a115757.
    1. Best LG, North KE, Tracy RP, Lee ET, Howard BV, Palmieri V, MacCluer JW. Genetic determination of acute phase reactant levels: the strong heart study. Hum Hered. 2004;58(2):112–116. doi: 10.1159/000083032.
    1. Chinali M, de Simone G, Roman MJ, Lee ET, Best LG, Howard BV, Devereux RB. Impact of obesity on cardiac geometry and function in a population of adolescents: the Strong Heart Study. J Am Coll Cardiol. 2006;47(11):2267–2273. doi: 10.1016/j.jacc.2006.03.004.
    1. Grundy SM, Brewer HB, Jr, Cleeman JI, Smith SC, Jr, Lenfant C. Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation. 2004;109(3):433–438. doi: 10.1161/01.CIR.0000111245.75752.C6.
    1. Ferrara LA, Capaldo B, Mancusi C, Lee ET, Howard BV, Devereux RB, de SG. Cardiometabolic risk in overweight subjects with or without relative fat-free mass deficiency: the Strong Heart Study. Nutr Metab Cardiovasc Dis. 2014;24(3):271–276. doi: 10.1016/j.numecd.2013.08.009.
    1. Stolarczyk LM, Heyward VH, Hicks VL, Baumgartner RN. Predictive accuracy of bioelectrical impedance in estimating body composition of Native American women. Am J ClinNutr. 1994;59(5):964–970.
    1. Association AD. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2007;30(Suppl 1):S42–S47. doi: 10.2337/dc07-S042.
    1. Levey AS, Coresh J, Greene T, Stevens LA, Zhang YL, Hendriksen S, Kusek JW, Van Lente F. Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Ann Intern Med. 2006;145(4):247–254. doi: 10.7326/0003-4819-145-4-200608150-00004.
    1. Devereux RB, Roman MJ, de Simone G, O’Grady MJ, Paranicas M, Yeh JL, Fabsitz RR, Howard BV. Relations of left ventricular mass to demographic and hemodynamic variables in American Indians: the Strong Heart Study. Circulation. 1997;96(5):1416–1423. doi: 10.1161/01.CIR.96.5.1416.
    1. Devereux RB, Roman MJ, Palmieri V, Liu JE, Lee ET, Best LG, Fabsitz RR, Rodeheffer RJ, Howard BV. Prognostic implications of ejection fraction from linear echocardiographic dimensions: the Strong Heart Study. Am Heart J. 2003;146(3):527–534. doi: 10.1016/S0002-8703(03)00229-1.
    1. Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N. Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol. 1986;57(6):450–458. doi: 10.1016/0002-9149(86)90771-X.
    1. de Simone G, Kizer JR, Chinali M, Roman MJ, Bella JN, Best LG, Lee ET, Devereux RB. Normalization for body size and population-attributable risk of left ventricular hypertrophy: the Strong Heart Study. Am J Hypertens. 2005;18(2):191–196. doi: 10.1016/j.amjhyper.2004.08.032.
    1. de Simone G, Daniels SR, Kimball TR, Roman MJ, Romano C, Chinali M, Galderisi M, Devereux RB. Evaluation of concentric left ventricular geometry in humans: evidence for age-related systematic underestimation. Hypertension. 2005;45(1):64–68. doi: 10.1161/01.HYP.0000150108.37527.57.
    1. Palmieri V, Dahlof B, DeQuattro V, Sharpe N, Bella JN, de Simone G, Paranicas M, Fishman D, Devereux RB. Reliability of echocardiographic assessment of left ventricular structure and function: the PRESERVE study. Prospective randomized study evaluating regression of ventricular enlargement [see comments] J Am Coll Cardiol. 1999;34(5):1625–1632. doi: 10.1016/S0735-1097(99)00396-4.
    1. Canciello G, de Simone G, Izzo R, Giamundo A, Pacelli F, Mancusi C, Galderisi M, Trimarco B, Losi MA. Validation of left atrial volume estimation by left atrial diameter from the parasternal long-axis view. J Am Soc Echocardiogr. 2017;30(3):262–269. doi: 10.1016/j.echo.2016.11.017.
    1. Kuznetsova T, Haddad F, Tikhonoff V, Kloch-Badelek M, Ryabikov A, Knez J, Malyutina S, Stolarz-Skrzypek K, Thijs L, Schnittger I, et al. Impact and pitfalls of scaling of left ventricular and atrial structure in population-based studies. J Hypertens. 2016;34(6):1186–1194. doi: 10.1097/HJH.0000000000000922.
    1. De Marco M, de Simone G, Roman MJ, Chinali M, Lee ET, Calhoun D, Howard BV, Devereux RB. Cardiac geometry and function in diabetic or prediabetic adolescents and young adults: the Strong Heart Study. Diabetes Care. 2011;34(10):2300–2305. doi: 10.2337/dc11-0191.
    1. Barnard J, Meng XL. Applications of multiple imputation in medical studies: from AIDS to NHANES. Stat Methods Med Res. 1999;8(1):17–36. doi: 10.1177/096228029900800103.
    1. de Simone G, Izzo R, Losi MA, Stabile E, Rozza F, Canciello G, Mancusi C, Trimarco V, De Luca N, Trimarco B. Depressed myocardial energetic efficiency is associated with increased cardiovascular risk in hypertensive left ventricular hypertrophy. J Hypertens. 2016;34(9):1846–1853. doi: 10.1097/HJH.0000000000001007.
    1. Laaksonen DE, Lakka HM, Niskanen LK, Kaplan GA, Salonen JT, Lakka TA. Metabolic syndrome and development of diabetes mellitus: application and validation of recently suggested definitions of the metabolic syndrome in a prospective cohort study. Am J Epidemiol. 2002;156(11):1070–1077. doi: 10.1093/aje/kwf145.
    1. Alexander CM, Landsman PB, Teutsch SM, Haffner SM. NCEP-defined metabolic syndrome, diabetes, and prevalence of coronary heart disease among NHANES III participants age 50 years and older. Diabetes. 2003;52(5):1210–1214. doi: 10.2337/diabetes.52.5.1210.
    1. Howard BV, Best LG, Galloway JM, Howard WJ, Jones K, Lee ET, Ratner RE, Resnick HE, Devereux RB. Coronary heart disease risk equivalence in diabetes depends on concomitant risk factors. Diabetes Care. 2006;29(2):391–397. doi: 10.2337/diacare.29.02.06.dc05-1299.
    1. de Simone G, Devereux RB, Chinali M, Best LG, Lee ET, Galloway JM, Resnick HE. Prognostic impact of metabolic syndrome by different definitions in a population with high prevalence of obesity and diabetes: the Strong Heart Study. Diabetes Care. 2007;30(7):1851–1856. doi: 10.2337/dc06-2152.
    1. Gomez-Marcos MA, Recio-Rodriguez JI, Patino-Alonso MC, Agudo-Conde C, Rodriguez-Sanchez E, Maderuelo-Fernandez JA, Gomez-Sanchez L, Gomez-Sanchez M, Garcia-Ortiz L, Group LD. Evolution of target organ damage and haemodynamic parameters over 4 years in patients with increased insulin resistance: the LOD-DIABETES prospective observational study. BMJ Open. 2016;6(6):e010400. doi: 10.1136/bmjopen-2015-010400.
    1. Gomez-Marcos MA, Recio-Rodriguez JI, Patino-Alonso MC, Agudo-Conde C, Gomez-Sanchez L, Gomez-Sanchez M, Rodriguez-Sanchez E, Maderuelo-Fernandez JA, Garcia-Ortiz L, Group LD. Cardio-ankle vascular index is associated with cardiovascular target organ damage and vascular structure and function in patients with diabetes or metabolic syndrome, LOD-DIABETES study: a case series report. Cardiovasc Diabetol. 2015;14:7. doi: 10.1186/s12933-014-0167-y.
    1. de Simone G, Arnett DK, Chinali M, De MM, Rao DC, Kraja AT, Hunt SC, Devereux RB. Partial normalization of components of metabolic syndrome does not influence prevalent echocardiographic abnormalities: the HyperGEN study. Nutr Metab Cardiovasc Dis. 2013;23(1):38–45. doi: 10.1016/j.numecd.2011.02.004.
    1. de Simone G, Devereux RB, Izzo R, Girfoglio D, Lee ET, Howard BV, Roman MJ. Lack of reduction of left ventricular mass in treated hypertension: the strong heart study. J Am Heart Assoc. 2013;2(3):e000144. doi: 10.1161/JAHA.113.000144.
    1. Lonnebakken MT, Izzo R, Mancusi C, Gerdts E, Losi MA, Canciello G, Giugliano G, De Luca N, Trimarco B, de Simone G. Left ventricular hypertrophy regression during antihypertensive treatment in an outpatient clinic (the Campania Salute Network) J Am Heart Assoc. 2017;6(3):004. doi: 10.1161/JAHA.116.004152.
    1. de Simone G, Devereux RB, Chinali M, Roman MJ, Best LG, Welty TK, Lee ET, Howard BV. Risk factors for arterial hypertension in adults with initial optimal blood pressure: the Strong Heart Study. Hypertension. 2006;47(2):162–167. doi: 10.1161/01.HYP.0000199103.40105.b5.
    1. Bertoni AG, Burke GL, Owusu JA, Carnethon MR, Vaidya D, Barr RG, Jenny NS, Ouyang P, Rotter JI. Inflammation and the incidence of type 2 diabetes: the Multi-Ethnic Study of Atherosclerosis (MESA) Diabetes Care. 2010;33(4):804–810. doi: 10.2337/dc09-1679.
    1. Spranger J, Kroke A, Mohlig M, Hoffmann K, Bergmann MM, Ristow M, Boeing H, Pfeiffer AF. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes. 2003;52(3):812–817. doi: 10.2337/diabetes.52.3.812.
    1. Papadopoulos DP, Makris TK. Masked hypertension definition, impact, outcomes: a critical review. J Clin Hypertens (Greenwich) 2007;9(12):956–963. doi: 10.1111/j.1524-6175.2007.07418.x.
    1. Gomez-Marcos MA, Recio-Rodriguez JI, Gomez-Sanchez L, Agudo-Conde C, Rodriguez-Sanchez E, Maderuelo-Fernandez J, Gomez-Sanchez M, Garcia-Ortiz L, Group LD. Gender differences in the progression of target organ damage in patients with increased insulin resistance: the LOD-DIABETES study. Cardiovasc Diabetol. 2015;14:132. doi: 10.1186/s12933-015-0293-1.
    1. de Simone G, Pasanisi F, Ferrara AL, Roman MJ, Lee ET, Contaldo F, Howard BV, Devereux RB. Relative fat-free mass deficiency and left ventricular adaptation to obesity: the Strong Heart Study. Int J Cardiol. 2013;168(2):729–733. doi: 10.1016/j.ijcard.2012.09.055.

Source: PubMed

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